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Isolation, Culture, and Immunostaining of Skeletal Muscle Myofibers from Wildtype and Nestin-GFP Mice as a Means to Analyze Satellite Cells

  • Pascal Stuelsatz
  • Paul Keire
  • Zipora Yablonka-ReuveniEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1556)

Abstract

Multinucleated myofibers, the functional contractile units of adult skeletal muscle, harbor mononuclear Pax7+ myogenic progenitors on their surface between the myofiber basal lamina and plasmalemma. These progenitors, known as satellite cells, are the primary myogenic stem cells in adult muscle. This chapter describes our laboratory protocols for isolating, culturing, and immunostaining intact myofibers from mouse skeletal muscle as a means for studying satellite cell dynamics. The first protocol discusses myofiber isolation from the flexor digitorum brevis (FDB) muscle. These short myofibers are plated in dishes coated with PureCol collagen (formerly known as Vitrogen) and maintained in a mitogen-poor medium (± supplemental growth factors). Employing such conditions, satellite cells remain at the surface of the parent myofiber while synchronously undergoing a limited number of proliferative cycles and rapidly differentiate. The second protocol discusses the isolation of longer myofibers from the extensor digitorum longus (EDL) muscle. These EDL myofibers are routinely plated individually as adherent myofibers in wells coated with Matrigel and maintained in a mitogen-rich medium, conditions in which satellite cells migrate away from the parent myofiber, proliferate extensively, and generate numerous differentiating progeny. Alternatively, these EDL myofibers can be plated as non-adherent myofibers in uncoated wells and maintained in a mitogen-poor medium (± supplemental growth factors), conditions that retain satellite cell progeny at the myofiber niche similar to the FDB myofiber cultures. However, the adherent myofiber format is our preferred choice for monitoring satellite cells in freshly isolated (Time 0) myofibers. We conclude this chapter by promoting the Nestin-GFP transgenic mouse as an efficient tool for direct analysis of satellite cells in isolated myofibers. While satellite cells have been often detected by their expression of the Pax7 protein or the Myf5nLacZ knockin reporter (approaches that are also detailed herein), the Nestin-GFP reporter distinctively permits quantification of satellite cells in live myofibers, which enables linking initial Time 0 numbers and subsequent performance upon culturing. We additionally point out to the implementation of the Nestin-GFP transgene for monitoring other selective cell lineages as illustrated by GFP expression in capillaries, endothelial tubes and neuronal cells. Myofibers from other types of muscles, such as diaphragm, masseter, and extraocular, can also be isolated and analyzed using protocols described herein. Collectively, this chapter provides essential tools for studying satellite cells in their native position and their interplay with the parent myofiber.

Key words

Skeletal muscle Satellite cells Isolated myofiber Flexor digitorum brevis Extensor digitorum longus Diaphragm Masseter Extraocular muscles Pax7 MyoD Myogenin Nestin-GFP Myf5nLacZ MLC3F-nLacZ 3F-nlacZ-2E 

Notes

Acknowledgments

The methods and results summarized in the current chapter reflect the culmination of continuous updates during many years of research. Our current research is supported by grants to Z.Y.R. from the National Institutes of Health (AG035377, NS090051, NS088804). Pascal Stuelsatz is supported by an AFM-telethon fellowship (#18574). The authors are additionally grateful to the granting agencies (MDA, AHA, USDA-NRI, NIH) that have funded this research in the past and to our former members of our laboratory (Antony Rivera, Gabi Shefer, Andrew Shearer, and Elena Danoviz) for their valuable contributions.

References

  1. 1.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495CrossRefGoogle Scholar
  2. 2.
    Yablonka-Reuveni Z (2011) The skeletal muscle satellite cell: still young and fascinating at 50. J Histochem Cytochem 59:1041–1059PubMedPubMedCentralGoogle Scholar
  3. 3.
    Montarras D, L’Honore A, Buckingham M (2013) Lying low but ready for action: the quiescent muscle satellite cell. FEBS J 280:4036–4050PubMedPubMedCentralGoogle Scholar
  4. 4.
    Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–435PubMedGoogle Scholar
  5. 5.
    Schultz E, Gibson MC, Champion T (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206:451–456PubMedPubMedCentralGoogle Scholar
  6. 6.
    White RB, Bierinx AS, Gnocchi VF, Zammit PS (2010) Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol 10:21PubMedPubMedCentralGoogle Scholar
  7. 7.
    Fry CS, Lee JD, Mula J, Kirby TJ, Jackson JR, Liu F, Yang L, Mendias CL, Dupont-Versteegden EE, McCarthy JJ, Peterson CA (2015) Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 21:76–80PubMedGoogle Scholar
  8. 8.
    Keefe AC, Lawson JA, Flygare SD, Fox ZD, Colasanto MP, Mathew SJ, Yandell M, Kardon G (2015) Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun 6:7087PubMedPubMedCentralGoogle Scholar
  9. 9.
    Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551PubMedPubMedCentralGoogle Scholar
  10. 10.
    Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54:1177–1191PubMedGoogle Scholar
  11. 11.
    Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646PubMedPubMedCentralGoogle Scholar
  12. 12.
    Grounds MD, Yablonka-Reuveni Z (1993) Molecular and cell biology of skeletal muscle regeneration. Mol Cell Biol Hum Dis Ser 3:210–256PubMedGoogle Scholar
  13. 13.
    Day K, Shefer G, Shearer A, Yablonka-Reuveni Z (2010) The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 340:330–343PubMedPubMedCentralGoogle Scholar
  14. 14.
    Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456:502–506PubMedPubMedCentralGoogle Scholar
  15. 15.
    Dumont NA, Wang YX, Rudnicki MA (2015) Intrinsic and extrinsic mechanisms regulating satellite cell function. Development 142:1572–1581PubMedPubMedCentralGoogle Scholar
  16. 16.
    Shefer G, Yablonka-Reuveni Z (2008) Ins and outs of satellite cell myogenesis: the role of the ruling growth factors. In: Schiaffino S, Partridge T (eds) Skeletal muscle repair and regeneration, Advances in muscle research, vol 3. Springer, Dordrecht, Netherlands, pp 107–144Google Scholar
  17. 17.
    Morgan JE, Zammit PS (2010) Direct effects of the pathogenic mutation on satellite cell function in muscular dystrophy. Exp Cell Res 316:3100–3108PubMedGoogle Scholar
  18. 18.
    Yablonka-Reuveni Z, Day K (2010) Skeletal muscle stem cells in the spotlight: the satellite cell. In: Cohen I, Gaudette G (eds) Regenerating the heart: stem cells and the cardiovascular system, Stem cell biology and regenerative medicine series. Humana Press, Springer, pp 173–200Google Scholar
  19. 19.
    Muir AR, Kanji AH, Allbrook D (1965) The structure of the satellite cells in skeletal muscle. J Anat 99:435–444PubMedPubMedCentralGoogle Scholar
  20. 20.
    Yablonka-Reuveni Z (1995) Development and postnatal regulation of adult myoblasts. Microsc Res Tech 30:366–380PubMedPubMedCentralGoogle Scholar
  21. 21.
    Boldrin L, Muntoni F, Morgan JE (2010) Are human and mouse satellite cells really the same? J Histochem Cytochem 58:941–955PubMedPubMedCentralGoogle Scholar
  22. 22.
    Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786PubMedPubMedCentralGoogle Scholar
  23. 23.
    Kawakami A, Kimura-Kawakami M, Nomura T, Fujisawa H (1997) Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech Dev 66:119–130PubMedGoogle Scholar
  24. 24.
    Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294:50–66PubMedPubMedCentralGoogle Scholar
  25. 25.
    Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS One 5:e13307PubMedPubMedCentralGoogle Scholar
  26. 26.
    Allouh MZ, Yablonka-Reuveni Z, Rosser BW (2008) Pax7 reveals a greater frequency and concentration of satellite cells at the ends of growing skeletal muscle fibers. J Histochem Cytochem 56:77–87PubMedPubMedCentralGoogle Scholar
  27. 27.
    Lindstrom M, Thornell LE (2009) New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132:141–157PubMedGoogle Scholar
  28. 28.
    Reimann J, Brimah K, Schroder R, Wernig A, Beauchamp JR, Partridge TA (2004) Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315:233–242PubMedGoogle Scholar
  29. 29.
    Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309:2064–2067PubMedPubMedCentralGoogle Scholar
  30. 30.
    Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234PubMedPubMedCentralGoogle Scholar
  31. 31.
    Day K, Shefer G, Richardson JB, Enikolopov G, Yablonka-Reuveni Z (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev Biol 304:246–259PubMedPubMedCentralGoogle Scholar
  32. 32.
    Stuelsatz P, Shearer A, Li Y, Muir LA, Ieronimakis N, Shen QW, Kirillova I, Yablonka-Reuveni Z (2015) Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency. Dev Biol 397:31–44PubMedGoogle Scholar
  33. 33.
    Shefer G, Rauner G, Stuelsatz P, Benayahu D, Yablonka-Reuveni Z (2013) Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice. FEBS J 280:4063–4073PubMedPubMedCentralGoogle Scholar
  34. 34.
    Yablonka-Reuveni Z, Danoviz ME, Phelps M, Stuelsatz P (2015) Myogenic-specific ablation of Fgfr1 impairs FGF2-mediated proliferation of satellite cells at the myofiber niche but does not abolish the capacity for muscle regeneration. Front Aging Neurosci 7:85PubMedPubMedCentralGoogle Scholar
  35. 35.
    Yablonka-Reuveni Z, Day K, Vine A, Shefer G (2008) Defining the transcriptional signature of skeletal muscle stem cells. J Anim Sci 86:E207–E216PubMedGoogle Scholar
  36. 36.
    Yablonka-Reuveni Z, Rivera AJ (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164:588–603PubMedPubMedCentralGoogle Scholar
  37. 37.
    Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357PubMedPubMedCentralGoogle Scholar
  38. 38.
    Day K, Paterson B, Yablonka-Reuveni Z (2009) A distinct profile of myogenic regulatory factor detection within Pax7+ cells at S phase supports a unique role of Myf5 during posthatch chicken myogenesis. Dev Dyn 238:1001–1009PubMedPubMedCentralGoogle Scholar
  39. 39.
    Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, Reshef R, Rozenboim I, Wleklinski-Lee M, Yablonka-Reuveni Z (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231:489–502PubMedGoogle Scholar
  40. 40.
    Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289–301PubMedPubMedCentralGoogle Scholar
  41. 41.
    Yablonka-Reuveni Z (2004) Isolation and culture of myogenic stem cells. In: Lanza R, Blau D, Melton D et al (eds) Handbook of Stem Cells—Vol 2: Adult and Fetal Stem Cells. Elsevier, San DiegoGoogle Scholar
  42. 42.
    Danoviz ME, Yablonka-Reuveni Z (2012) Skeletal muscle satellite cells: background and methods for isolation and analysis in a primary culture system. Methods Mol Biol 798:21–52PubMedPubMedCentralGoogle Scholar
  43. 43.
    Yablonka-Reuveni Z, Quinn LS, Nameroff M (1987) Isolation and clonal analysis of satellite cells from chicken pectoralis muscle. Dev Biol 119:252–259PubMedPubMedCentralGoogle Scholar
  44. 44.
    Kastner S, Elias MC, Rivera AJ, Yablonka-Reuveni Z (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J Histochem Cytochem 48:1079–1096PubMedGoogle Scholar
  45. 45.
    Ieronimakis N, Balasundaram G, Rainey S, Srirangam K, Yablonka-Reuveni Z, Reyes M (2010) Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS One 5:e10920PubMedPubMedCentralGoogle Scholar
  46. 46.
    Bekoff A, Betz W (1977) Properties of isolated adult rat muscle fibres maintained in tissue culture. J Physiol 271:537–547PubMedPubMedCentralGoogle Scholar
  47. 47.
    Bischoff R (1986) Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol 115:129–139PubMedPubMedCentralGoogle Scholar
  48. 48.
    Bischoff R (1989) Analysis of muscle regeneration using single myofibers in culture. Med Sci Sports Exerc 21:S164–S172PubMedGoogle Scholar
  49. 49.
    Yablonka-Reuveni Z, Rivera AJ (1997) Proliferative dynamics and the role of FGF2 during myogenesis of rat satellite cells on isolated fibers. Basic Appl Myol 7:189–202PubMedPubMedCentralGoogle Scholar
  50. 50.
    Yablonka-Reuveni Z, Anderson JE (2006) Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev Dyn 235:203–212PubMedGoogle Scholar
  51. 51.
    Yablonka-Reuveni Z, Rudnicki MA, Rivera AJ, Primig M, Anderson JE, Natanson P (1999) The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev Biol 210:440–455PubMedPubMedCentralGoogle Scholar
  52. 52.
    Rosenblatt JD, Lunt AI, Parry DJ, Partridge TA (1995) Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev Biol Anim 31:773–779PubMedPubMedCentralGoogle Scholar
  53. 53.
    Rosenblatt JD, Parry DJ, Partridge TA (1996) Phenotype of adult mouse muscle myoblasts reflects their fiber type of origin. Differentiation 60:39–45PubMedGoogle Scholar
  54. 54.
    Stuelsatz P, Keire P, Almuly R, Yablonka-Reuveni Z (2012) A contemporary atlas of the mouse diaphragm: myogenicity, vascularity, and the Pax3 connection. J Histochem Cytochem 60:638–657PubMedPubMedCentralGoogle Scholar
  55. 55.
    Yablonka-Reuveni Z, Seger R, Rivera AJ (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47:23–42PubMedGoogle Scholar
  56. 56.
    Shefer G, Partridge TA, Heslop L, Gross JG, Oron U, Halevy O (2002) Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 115:1461–1469PubMedGoogle Scholar
  57. 57.
    Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311–324PubMedGoogle Scholar
  58. 58.
    Tajbakhsh S, Rocancourt D, Buckingham M (1996) Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 384:266–270PubMedGoogle Scholar
  59. 59.
    Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89:127–138PubMedGoogle Scholar
  60. 60.
    Kelly R, Alonso S, Tajbakhsh S, Cossu G, Buckingham M (1995) Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J Cell Biol 129:383–396PubMedGoogle Scholar
  61. 61.
    Chapman VM, Miller DR, Armstrong D, Caskey CT (1989) Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc Natl Acad Sci U S A 86:1292–1296PubMedPubMedCentralGoogle Scholar
  62. 62.
    Im WB, Phelps SF, Copen EH, Adams EG, Slightom JL, Chamberlain JS (1996) Differential expression of dystrophin isoforms in strains of mdx mice with different mutations. Hum Mol Genet 5:1149–1153PubMedGoogle Scholar
  63. 63.
    Banks GB, Combs AC, Chamberlain JS (2010) Sequencing protocols to genotype mdx, mdx(4cv), and mdx(5cv) mice. Muscle Nerve 42:268–270PubMedPubMedCentralGoogle Scholar
  64. 64.
    Lu QL, Morris GE, Wilton SD, Ly T, Artem’yeva OV, Strong P, Partridge TA (2000) Massive idiosyncratic exon skipping corrects the nonsense mutation in dystrophic mouse muscle and produces functional revertant fibers by clonal expansion. J Cell Biol 148:985–996PubMedPubMedCentralGoogle Scholar
  65. 65.
    Arpke RW, Darabi R, Mader TL, Zhang Y, Toyama A, Lonetree CL, Nash N, Lowe DA, Perlingeiro RC, Kyba M (2013) A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells 31:1611–1620PubMedPubMedCentralGoogle Scholar
  66. 66.
    Danko I, Chapman V, Wolff JA (1992) The frequency of revertants in mdx mouse genetic models for Duchenne muscular dystrophy. Pediatr Res 32:128–131PubMedGoogle Scholar
  67. 67.
    Decrouy A, Renaud JM, Davis HL, Lunde JA, Dickson G, Jasmin BJ (1997) Mini-dystrophin gene transfer in mdx4cv diaphragm muscle fibers increases sarcolemmal stability. Gene Ther 4:401–408PubMedGoogle Scholar
  68. 68.
    Judge LM, Haraguchiln M, Chamberlain JS (2006) Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J Cell Sci 119:1537–1546PubMedGoogle Scholar
  69. 69.
    Dias P, Parham DM, Shapiro DN, Tapscott SJ, Houghton PJ (1992) Monoclonal antibodies to the myogenic regulatory protein MyoD1: epitope mapping and diagnostic utility. Cancer Res 52:6431–6439PubMedGoogle Scholar
  70. 70.
    Wright WE, Binder M, Funk W (1991) Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol Cell Biol 11:4104–4110PubMedPubMedCentralGoogle Scholar
  71. 71.
    Wright WE, Dac-Korytko I, Farmer K (1996) Monoclonal antimyogenin antibodies define epitopes outside the bHLH domain where binding interferes with protein-protein and protein-DNA interactions. Dev Genet 19:131–138PubMedGoogle Scholar
  72. 72.
    Shefer G, Wleklinski-Lee M, Yablonka-Reuveni Z (2004) Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. J Cell Sci 117:5393–5404PubMedGoogle Scholar
  73. 73.
    Anderson JE, McIntosh LM, Moor AN, Yablonka-Reuveni Z (1998) Levels of MyoD protein expression following injury of mdx and normal limb muscle are modified by thyroid hormone. J Histochem Cytochem 46:59–67PubMedGoogle Scholar
  74. 74.
    Gause KC, Homma MK, Licciardi KA, Seger R, Ahn NG, Peterson MJ, Krebs EG, Meier KE (1993) Effects of phorbol ester on mitogen-activated protein kinase kinase activity in wild-type and phorbol ester-resistant EL4 thymoma cells. J Biol Chem 268:16124–16129PubMedGoogle Scholar
  75. 75.
    Seger R, Seger D, Reszka AA, Munar ES, Eldar-Finkelman H, Dobrowolska G, Jensen AM, Campbell JS, Fischer EH, Krebs EG (1994) Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH 3T3 cells. Evidence that MAPKK involvement in cellular proliferation is regulated by phosphorylation of serine residues in its kinase subdomains VII and VIII. J Biol Chem 269:25699–25709PubMedGoogle Scholar
  76. 76.
    Greene EC (1963) Anatomy of the rat. Hafner Publishing Company, New York, NYGoogle Scholar
  77. 77.
    Wozniak AC, Pilipowicz O, Yablonka-Reuveni Z, Greenway S, Craven S, Scott E, Anderson JE (2003) C-Met expression and mechanical activation of satellite cells on cultured muscle fibers. J Histochem Cytochem 51:1437–1445PubMedPubMedCentralGoogle Scholar
  78. 78.
    Michalczyk K, Ziman M (2005) Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 20:665–671PubMedGoogle Scholar
  79. 79.
    Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM (2004) Nestin expression—a property of multi-lineage progenitor cells? Cell Mol Life Sci 61:2510–2522PubMedGoogle Scholar
  80. 80.
    Shefer G, Wleklinski-Lee M, Yablonka-Reuveni Z (2004) Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. J Cell Sci 117:5393–5404PubMedGoogle Scholar
  81. 81.
    Kania G, Blyszczuk P, Czyz J, Navarrete-Santos A, Wobus AM (2003) Differentiation of mouse embryonic stem cells into pancreatic and hepatic cells. Methods Enzymol 365:287–303PubMedGoogle Scholar
  82. 82.
    Vogel W, Grunebach F, Messam CA, Kanz L, Brugger W, Buhring HJ (2003) Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 88:126–133PubMedGoogle Scholar
  83. 83.
    Amoh Y, Li L, Katsuoka K, Penman S, Hoffman RM (2005) Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc Natl Acad Sci U S A 102:5530–5534PubMedPubMedCentralGoogle Scholar
  84. 84.
    Davidoff MS, Middendorff R, Enikolopov G, Riethmacher D, Holstein AF, Muller D (2004) Progenitor cells of the testosterone-producing Leydig cells revealed. J Cell Biol 167:935–944PubMedPubMedCentralGoogle Scholar
  85. 85.
    Asakura A, Komaki M, Rudnicki M (2001) Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68:245–253PubMedGoogle Scholar
  86. 86.
    Keire P, Shearer A, Shefer G, Yablonka-Reuveni Z (2013) Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol Biol 946:431–468PubMedPubMedCentralGoogle Scholar
  87. 87.
    Shefer G, Yablonka-Reuveni Z (2007) Reflections on lineage potential of skeletal muscle satellite cells: do they sometimes go MAD? Crit Rev Eukaryot Gene Expr 17:13–29PubMedPubMedCentralGoogle Scholar
  88. 88.
    Starkey JD, Yamamoto M, Yamamoto S, Goldhamer DJ (2011) Skeletal muscle satellite cells are committed to myogenesis and do not spontaneously adopt nonmyogenic fates. J Histochem Cytochem 59:33–46PubMedPubMedCentralGoogle Scholar
  89. 89.
    Bischoff R (1986) A satellite cell mitogen from crushed adult muscle. Dev Biol 115:140–147PubMedGoogle Scholar
  90. 90.
    Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010PubMedPubMedCentralGoogle Scholar
  91. 91.
    Cossu G, Tajbakhsh S (2007) Oriented cell divisions and muscle satellite cell heterogeneity. Cell 129:859–861PubMedGoogle Scholar
  92. 92.
    Yablonka-Reuveni Z, Christ B, Benson JM (1998) Transitions in cell organization and in expression of contractile and extracellular matrix proteins during development of chicken aortic smooth muscle: evidence for a complex spatial and temporal differentiation program. Anat Embryol (Berl) 197:421–437Google Scholar
  93. 93.
    Yablonka-Reuveni Z, Nameroff M (1990) Temporal differences in desmin expression between myoblasts from embryonic and adult chicken skeletal muscle. Differentiation 45:21–28PubMedPubMedCentralGoogle Scholar
  94. 94.
    Yablonka-Reuveni Z, Schwartz SM, Christ B (1995) Development of chicken aortic smooth muscle: expression of cytoskeletal and basement membrane proteins defines two distinct cell phenotypes emerging from a common lineage. Cell Mol Biol Res 41:241–249PubMedGoogle Scholar
  95. 95.
    Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS (2010) Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol 337:29–41PubMedPubMedCentralGoogle Scholar
  96. 96.
    Zammit PS, Heslop L, Hudon V, Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281:39–49PubMedGoogle Scholar
  97. 97.
    Stuelsatz P, Yablonka-Reuveni Z (2016) Isolation of mouse periocular tissue for histological and immunostaining analyses of the extraocular muscles and their satellite cells. Methods Mol Biol 1460:101-127.Google Scholar
  98. 98.
    Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR (1982) Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21:6188–6193PubMedGoogle Scholar
  99. 99.
    Yablonka-Reuveni Z, Seifert RA (1993) Proliferation of chicken myoblasts is regulated by specific isoforms of platelet-derived growth factor: evidence for differences between myoblasts from mid and late stages of embryogenesis. Dev Biol 156:307–318PubMedGoogle Scholar
  100. 100.
    Yablonka-Reuveni Z (1995) Myogenesis in the chicken: the onset of differentiation of adult myoblasts is influenced by tissue factors. Basic Appl Myol 5:33–42PubMedPubMedCentralGoogle Scholar
  101. 101.
    O’Neill MC, Stockdale FE (1972) A kinetic analysis of myogenesis in vitro. J Cell Biol 52:52–65PubMedPubMedCentralGoogle Scholar
  102. 102.
    Gray, H. (1918) The muscles and fasciæ of the foot. In: Anatomy of the human body. Available via Bartleby.com. http://www.bartleby.com/107/131.html. Accessed 17 Nov 2016
  103. 103.
    Gray, H. (1918) Fig. 443. In: Anatomy of the human body. Available via Bartleby.com. http://www.bartleby.com/107/illus443.html. Accessed 17 Nov 2016
  104. 104.
    Gray, H. (1918) Fig. 437. In: Anatomy of the human body. Available via Bartleby.com. http://www.bartleby.com/107/illus437.html. Accessed 17 Nov 2016
  105. 105.
    Gray, H. (1918) Fig. 441. In: Anatomy of the Human Body. Available via Bartleby.com. http://www.bartleby.com/107/illus441.html. Accessed 17 Nov 2016
  106. 106.
    Gray, H. (1918) The muscles and fasciæ of the leg. In: Anatomy of the Human Body. Available via Bartleby.com. http://www.bartleby.com/107/129.html. Accessed 17 Nov 2016
  107. 107.
    Shefer G, Yablonka-Reuveni Z (2005) Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells. Methods Mol Biol 290:281–304PubMedPubMedCentralGoogle Scholar
  108. 108.
    Birbrair A, Wang ZM, Messi ML, Enikolopov GN, Delbono O (2011) Nestin-GFP transgene reveals neural precursor cells in adult skeletal muscle. PLoS One 6:e16816PubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  • Pascal Stuelsatz
    • 1
  • Paul Keire
    • 1
  • Zipora Yablonka-Reuveni
    • 1
    Email author
  1. 1.Department of Biological Structure, School of MedicineUniversity of WashingtonSeattleUSA

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